Spatial Sequence Coding Differs during Slow and Fast Gamma Rhythms in the Hippocampus

Neuron

Volumn 89, Issue 2, 2016, Pages 398-408

  Zheng, Chenguang ^a   Bieri, Kevin Wood ^a   Hsiao, Yi Tse ^a   Colgin, Laura Lee ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; FAST GAMMA RHYTHM; GAMMA RHYTHM; HIPPOCAMPUS; MALE; NERVE CELL MEMBRANE POTENTIAL; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; RAT; SLOW GAMMA RHYTHM; SPIKE WAVE; THETA RHYTHM; ACTION POTENTIAL; ANIMAL; LONG EVANS RAT; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; GAMMA RHYTHM; HIPPOCAMPUS; MALE; RATS; RATS, LONG-EVANS; THETA RHYTHM;

EID: 84961214132     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.12.005     Document Type: Article

References (56)

1. Ahmed O.J., Mehta M.R. Running speed alters the frequency of hippocampal gamma oscillations. J. Neurosci. 2012, 32:7373-7383.
2. Belluscio M.A., Mizuseki K., Schmidt R., Kempter R., Buzsáki G. Cross-frequency phase-phase coupling between θ and γ oscillations in the hippocampus. J. Neurosci. 2012, 32:423-435.
3. Bieri K.W., Bobbitt K.N., Colgin L.L. Slow and fast gamma rhythms coordinate different spatial coding modes in hippocampal place cells. Neuron 2014, 82:670-681.
4. Brown E.N., Frank L.M., Tang D., Quirk M.C., Wilson M.A. A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. J. Neurosci. 1998, 18:7411-7425.
5. Brun V.H., Otnass M.K., Molden S., Steffenach H.A., Witter M.P., Moser M.B., Moser E.I. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 2002, 296:2243-2246.
6. Buzsáki G., Leung L.W., Vanderwolf C.H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 1983, 287:139-171.
7. Cabral H.O., Vinck M., Fouquet C., Pennartz C.M., Rondi-Reig L., Battaglia F.P. Oscillatory dynamics and place field maps reflect hippocampal ensemble processing of sequence and place memory under NMDA receptor control. Neuron 2014, 81:402-415.
8. Carr M.F., Karlsson M.P., Frank L.M. Transient slow gamma synchrony underlies hippocampal memory replay. Neuron 2012, 75:700-713.
9. Chen Z., Resnik E., McFarland J.M., Sakmann B., Mehta M.R. Speed controls the amplitude and timing of the hippocampal gamma rhythm. PLoS ONE 2011, 6:e21408.
10. Colgin L.L., Moser E.I. Neuroscience: rewinding the memory record. Nature 2006, 440:615-617.
11. Colgin L.L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M.B., Moser E.I. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 2009, 462:353-357.
12. Csicsvari J., Hirase H., Czurkó A., Mamiya A., Buzsáki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving rat. J. Neurosci. 1999, 19:274-287.
13. Davidson T.J., Kloosterman F., Wilson M.A. Hippocampal replay of extended experience. Neuron 2009, 63:497-507.
14. Diba K., Buzsáki G. Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci. 2007, 10:1241-1242.
15. Dragoi G., Buzsáki G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 2006, 50:145-157.
16. English D.F., Peyrache A., Stark E., Roux L., Vallentin D., Long M.A., Buzsáki G. Excitation and inhibition compete to control spiking during hippocampal ripples: intracellular study in behaving mice. J. Neurosci. 2014, 34:16509-16517.
17. Feng T., Silva D., Foster D.J. Dissociation between the experience-dependent development of hippocampal theta sequences and single-trial phase precession. J. Neurosci. 2015, 35:4890-4902.
18. Foster D.J., Wilson M.A. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 2006, 440:680-683.
19. Foster D.J., Wilson M.A. Hippocampal theta sequences. Hippocampus 2007, 17:1093-1099.
20. Foster D.J., Knierim J.J. Sequence learning and the role of the hippocampus in rodent navigation. Curr. Opin. Neurobiol. 2012, 22:294-300.
21. Gupta A.S., van der Meer M.A., Touretzky D.S., Redish A.D. Segmentation of spatial experience by hippocampal θ sequences. Nat. Neurosci. 2012, 15:1032-1039.
22. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
23. Harris K.D., Csicsvari J., Hirase H., Dragoi G., Buzsáki G. Organization of cell assemblies in the hippocampus. Nature 2003, 424:552-556.
24. Hasselmo M.E., Bodelón C., Wyble B.P. A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Comput. 2002, 14:793-817.
25. Jensen O., Lisman J.E. Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn. Mem. 1996, 3:279-287.
26. Jensen O., Lisman J.E. Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. J. Neurophysiol. 2000, 83:2602-2609.
27. Johnson A., Redish A.D. Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 2007, 27:12176-12189.
28. Kemere C., Carr M.F., Karlsson M.P., Frank L.M. Rapid and continuous modulation of hippocampal network state during exploration of new places. PLoS ONE 2013, 8:e73114.
29. Kempter R., Leibold C., Buzsáki G., Diba K., Schmidt R. Quantifying circular-linear associations: hippocampal phase precession. J. Neurosci. Methods 2012, 207:113-124.
30. Lee A.K., Wilson M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 2002, 36:1183-1194.
31. Levy W.B. A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus 1996, 6:579-590.
32. Lisman J. The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme. Hippocampus 2005, 15:913-922.
33. Lisman J.E., Jensen O. The theta-gamma neural code. Neuron 2013, 77:1002-1016.
34. Muller R.U., Kubie J.L. The firing of hippocampal place cells predicts the future position of freely moving rats. J. Neurosci. 1989, 9:4101-4110.
35. Nádasdy Z., Hirase H., Czurkó A., Csicsvari J., Buzsáki G. Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci. 1999, 19:9497-9507.
36. O'Keefe J. Place units in the hippocampus of the freely moving rat. Exp. Neurol. 1976, 51:78-109.
37. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971, 34:171-175.
38. O'Keefe J.M., Nadel L. The Hippocampus as a Cognitive Map 1978, Oxford University Press.
39. O'Keefe J., Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 1993, 3:317-330.
40. Penttonen M., Kamondi A., Acsády L., Buzsáki G. Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo. Eur. J. Neurosci. 1998, 10:718-728.
41. Pfeiffer B.E., Foster D.J. Hippocampal place-cell sequences depict future paths to remembered goals. Nature 2013, 497:74-79.
42. Pfeiffer B.E., Foster D.J. Autoassociative dynamics in the generation of sequences of hippocampal place cells. Science 2015, 349:180-183.
43. Schlesiger M.I., Cannova C.C., Boublil B.L., Hales J.B., Mankin E.A., Brandon M.P., Leutgeb J.K., Leibold C., Leutgeb S. The medial entorhinal cortex is necessary for temporal organization of hippocampal neuronal activity. Nat. Neurosci. 2015, 18:1123-1132.
44. Schomburg E.W., Fernández-Ruiz A., Mizuseki K., Berényi A., Anastassiou C.A., Koch C., Buzsáki G. Theta phase segregation of input-specific gamma patterns in entorhinal-hippocampal networks. Neuron 2014, 84:470-485.
45. Senior T.J., Huxter J.R., Allen K., O'Neill J., Csicsvari J. Gamma oscillatory firing reveals distinct populations of pyramidal cells in the CA1 region of the hippocampus. J. Neurosci. 2008, 28:2274-2286.
46. Siegel M., Warden M.R., Miller E.K. Phase-dependent neuronal coding of objects in short-term memory. Proc. Natl. Acad. Sci. USA 2009, 106:21341-21346.
47. Skaggs W.E., McNaughton B.L., Wilson M.A., Barnes C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 1996, 6:149-172.
48. Soltesz I., Deschênes M. Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J. Neurophysiol. 1993, 70:97-116.
49. Takahashi M., Nishida H., Redish A.D., Lauwereyns J. Theta phase shift in spike timing and modulation of gamma oscillation: a dynamic code for spatial alternation during fixation in rat hippocampal area CA1. J. Neurophysiol. 2014, 111:1601-1614.
50. Wallenstein G.V., Hasselmo M.E. GABAergic modulation of hippocampal population activity: sequence learning, place field development, and the phase precession effect. J. Neurophysiol. 1997, 78:393-408.
51. Wallenstein G.V., Eichenbaum H., Hasselmo M.E. The hippocampus as an associator of discontiguous events. Trends Neurosci. 1998, 21:317-323.
52. Wikenheiser A.M., Redish A.D. Hippocampal theta sequences reflect current goals. Nat. Neurosci. 2015, 18:289-294.
53. Yamamoto J., Suh J., Takeuchi D., Tonegawa S. Successful execution of working memory linked to synchronized high-frequency gamma oscillations. Cell 2014, 157:845-857.
54. Zhang K., Ginzburg I., McNaughton B.L., Sejnowski T.J. Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J. Neurophysiol. 1998, 79:1017-1044.
55. Zhang S.J., Ye J., Miao C., Tsao A., Cerniauskas I., Ledergerber D., Moser M.B., Moser E.I. Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science 2013, 340:1232627.
56. Zheng C., Bieri K.W., Trettel S.G., Colgin L.L. The relationship between gamma frequency and running speed differs for slow and fast gamma rhythms in freely behaving rats. Hippocampus 2015, 25:924-938.